Emotion and cognition and the amygdala: from "what is it?" to "what's to be done?".

Abstract

The amygdala is a fascinating, complex structure that lies at the center of much of our current thinking about emotion. Here, I will review data that suggest that the amygdala is involved in several processes linked to determining what a stimulus is and what the organism should therefore do - the two questions that are part of the title. This piece will focus on three main aspects of amygdala function, namely attention, value representation, and decision making, by reviewing both non-human and human data. Two mechanisms of affective attention will be described. The first involves projections from the central nucleus of the amygdala to the basal forebrain, which has extensive and diffuse projections throughout the cortical mantle. The second involves projections from the basal amygdala to multiple levels across the visual cortex. I will also describe how the basolateral amygdala is important for the representation of value and in decision making. Overall, it will be argued that the amygdala plays a key role in solving the following problem: How can a limited-capacity information processing system that receives a constant stream of diverse inputs be designed to selectively process those inputs that are most significant to the objectives of the system? "What is it?" and "What's to be done?" processes can then be viewed as important building blocks in the construction of emotion, a process that is intertwined with cognition. Furthermore, answering the two questions directs how resources should be mobilized as the organism seeks out additional information from the environment.

Amygdala. Anatomically, the amygdala is a complex of more than a dozen nuclei. Here, we will focus on functions of the basolateral complex (including the lateral, basal, and accessory basal nuclei) and the central nucleus). The central nucleus (CE) and the basolateral complex (B: basal nucleus; L: lateral nucleus; AB: accessory basal nucleus), are shown among other amygdala nuclei (for the remaining abbreviations, see ()). Reproduced from () with permission.

Amygdala activation to neutral faces. Contrast of viewing neutral faces vs. viewing buildings during a one-back working memory task (N = 30). Robust differential responses were observed in the amygdala (approximately indicated by the blue circles), and extended dorsally into the basal forebrain, and even into the globus pallidus. Data from “localizer runs” re-analyzed from .

Basal forebrain modulation of sensory processing. The basal forebrain (blue ellipses) has widespread connections throughout the cortical mantle, including to sensory cortex. These latter projections are suggested to have an important role in influencing how sensory information is registered and processed. Here, the basal forebrain is represented only schematically and situated atop the amygdala. For the precise localization of the magnocellular cell groups in humans, see of ().

Ascending and descending projections of the central nucleus. The central nucleus influences information processing throughout cortex, an effect that is mediated via the basal forebrain. At the same time, descending projections via the hypothalamus and other brainstem sites leads to the mobilization of bodily resources. Both ascending and descending systems are suggested to contribute to affective attention. BF: basal forebrain; HYP: hypothalamus.

Attentional blink paradigm. (A) Participants were asked to report on the face stimulus (T1) and on whether the stream contained a house, a building, or no scene (T2). Houses or buildings were paired with mild electrical stimulation during an initial learning phase. During the main experimental phase, only trials in which no stimulation was administered were analyzed. (B) It was hypothesized that the link between responses evoked in the amygdala and behavior (i.e., detection of T2) was mediated via specific regions of visual cortex – in this case, the parahippocampal gyrus given its involvement in the processing of scenes and spatial layouts. It was further anticipated that this relationship would be observed in terms of mean responses (across participants; shown schematically in red and blue), but also in terms of moment-to-moment fluctuations in evoked brain responses and behavior (shown in purple). Reproduced from with permission.

Trial-by-trial analysis. (A) Logistic regression analysis of evoked responses in the right parahippocampal gyrus (PHG) as a function of affective significance (CS+ and CS−) for one individual (dichotomous variable: hits vs. misses). The slope of the logistic fit indicates the strength of the predictive effect. For clarity, only binned data for the CS+ condition are shown (red dots). (B) Mean logistic slopes across individuals for the parahippocampal gyrus. (C) The same analysis as in (A) but for the right amygdala (AMYG). (D) Mean logistic slopes across individuals for the amygdala. (E) The strength of the visual cortex-to-behavior relationship (as indexed via the slope of the logistic fit) was correlated with the magnitude of evoked responses in the amygdala: The stronger the response in the amygdala, the tighter the relationship between visual responses and behavior. Reproduced from with permission.

Competition in visual cortex. Competition is influenced by both bottom-up stimulus dimensions (e.g., stimulus contrast) and by top-down mechanisms that are dependent on task goals (e.g., “search for faces”). Importantly, competition is also influenced by the affective significance and value of items. The latter is suggested to be supported by several potentially parallel mechanisms that rely on the amygdala, orbitofrontal cortex, and pulvinar nucleus of the thalamus, among others. Overall, the processing of affectively significant items receives prioritized processing. Note that the contribution of the pulvinar is suggested to be indirect (green arrow), given that the “visual” pulvinar is separate from the more “associational” pulvinar, which is suggested to be more directly involved in determining value (see ).

Graded representation of value. (A) Cell responses during presentation of the visual CS stimulus from a cell that encoded negative value. (B) Cell responses during the “trace interval” (i.e., interval between the visual stimulus offset and outcome delivery [US]) from a cell that encoded positive value. Reproduced from with permission.